Light-Mediated Seed Germination: Connecting Phytochrome B to Gibberellic Acid
2012; Elsevier BV; Volume: 22; Issue: 4 Linguagem: Inglês
10.1016/j.devcel.2012.04.003
ISSN1878-1551
Autores Tópico(s)Photosynthetic Processes and Mechanisms
ResumoIn this issue of Developmental Cell, Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar uncover the mechanisms linking the light-regulated trigger and hormone-mediated induction of seed germination in Arabidopsis. When phytochrome B is activated by red light, seed germination is promoted by epigenetic transcriptional activation of gibberellic acid biosynthetic enzymes via histone demethylation. In this issue of Developmental Cell, Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar uncover the mechanisms linking the light-regulated trigger and hormone-mediated induction of seed germination in Arabidopsis. When phytochrome B is activated by red light, seed germination is promoted by epigenetic transcriptional activation of gibberellic acid biosynthetic enzymes via histone demethylation. We have all been taught that most plants use light as source of energy, allowing the fixing of atmospheric carbon into organic compounds such as sugars. Less well known, at least among the general public, is that plants also use light as a source of information, allowing for the adjustment of growth and development in response to changing environmental conditions. This process, termed photomorphogenesis, is regulated by a suite of photoreceptors that is not directly involved in the chemistry of photosynthesis (for review, see Kami et al., 2010Kami C. Lorrain S. Hornitschek P. Fankhauser C. Curr. Top. Dev. Biol. 2010; 91: 29-66Crossref PubMed Scopus (544) Google Scholar). Sixty years ago, Borthwick et al., 1952Borthwick H.A. Hendricks S.B. Parker M.W. Toole E.H. Toole V.K. Proc. Natl. Acad. Sci. USA. 1952; 38: 662-666Crossref PubMed Google Scholar demonstrated that red light could induce germination in a particular variety of lettuce seeds (cv. Grand Rapids) that had been presoaked in water in darkness and showed that far-red light (which is not absorbed during photosynthesis) could reverse this induction (Figure 1). This photomorphogenic response ultimately led to the identification and purification of the red/far-red absorbing photoreceptors called phytochromes (for "plant pigment"). The red/far-red control of lettuce seed germination has been used as a laboratory exercise to teach phytochrome-mediated photomorphogenesis for many years. This practice stopped as breeding efforts bypassed the need for light to germinate lettuce seeds. Recently, this laboratory exercise was resurrected with the identification of one Grand Rapids-derived variety, Waldman's Dark Green, which still maintains phytochrome-mediated regulation of seed germination (Neff et al., 2009Neff M.M. Sanderson L. Tedor D. Am. Biol. Teach. 2009; 71: 367-370Google Scholar). Light-mediated seed germination is generally associated with sun-loving small-seeded species such as lettuce and Arabidopsis. In addition to being a mechanism for avoiding germination in the shade of adult plants, the energy reserves in these seeds are not sufficient for elongation and emersion from deep in the soil. Light and water are not the only factors regulating seed germination. For many plants, seed germination is repressed by the hormone abscisic acid (ABA) and stimulated by another hormone, gibberellin (GA). In Arabidopsis, the activation of phytochrome leads to decreased levels of ABA and increased levels of GA, releasing the repression and allowing the stimulation of seed germination. In part, this GA-mediated stimulation of germination is caused by the phytochrome-mediated induction of transcript accumulation for two GA oxidase enzymes that metabolize bioactive GAs, GA3ox1, and GA3ox3 (for review, see Seo et al., 2009Seo M. Nambara E. Choi G. Yamaguchi S. Plant Mol. Biol. 2009; 69: 463-472Crossref PubMed Scopus (255) Google Scholar). Although the early steps in phytochrome signal transduction have been elucidated (see Kami et al., 2010Kami C. Lorrain S. Hornitschek P. Fankhauser C. Curr. Top. Dev. Biol. 2010; 91: 29-66Crossref PubMed Scopus (544) Google Scholar), as have the signaling steps downstream from GA perception (see Seo et al., 2009Seo M. Nambara E. Choi G. Yamaguchi S. Plant Mol. Biol. 2009; 69: 463-472Crossref PubMed Scopus (255) Google Scholar), making the direct molecular connection between these two pathways has, until now, been elusive. The findings of Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar, as reported in this issue of Developmental Cell, now add another foundational layer of knowledge on how light, via phytochromes, elevates GA levels to stimulate seed germination in Arabidopsis. Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar initiate these studies with the intent of characterizing putative histone arginine (HR) demethylases in Arabidopsis. In humans, the Jumonji C (JmjC) domain-containing protein, JMJD6, was reported to be an HR demethylase (Chang et al., 2007Chang B. Chen Y. Zhao Y. Bruick R.K. Science. 2007; 318: 444-447Crossref PubMed Scopus (521) Google Scholar). The Arabidopsis genome encodes 21 JmjC domain-containing proteins. Of these, Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar identify three proteins (JMJ20, JMJ21, and JMJ22) that are most similar to JMJD6. In their preliminary genetic analysis, the authors find that the jmj20-1 jmj22-1 double mutant confers reduced germination after a 1 to 5 min red-light treatment. They also observed that this germination defect can be rescued by 1 hr of exposure to red light or the application of GA. Together, these results suggest that the loss of JMJ20 and JMJ22 leads to a reduction in GA levels in association with the activity of a particular phytochrome, phytochrome B, which responds to red light (see Seo et al., 2009Seo M. Nambara E. Choi G. Yamaguchi S. Plant Mol. Biol. 2009; 69: 463-472Crossref PubMed Scopus (255) Google Scholar). When phytochrome B is inactive, it is sequestered in the cytoplasm and thus does not bind nuclear-localized proteins such as the basic helix-loop-helix transcription factor PHYTOCHROME-INTERACTING FACTOR 3-LIKE 5 (PIL5) (see Kami et al., 2010Kami C. Lorrain S. Hornitschek P. Fankhauser C. Curr. Top. Dev. Biol. 2010; 91: 29-66Crossref PubMed Scopus (544) Google Scholar). When present, PIL5 acts as a repressor of seed germination in part by upregulating a second nuclear localized protein, SOMNUS (SOM), also a repressor of seed germination (Park et al., 2011Park J. Lee N. Kim W. Lim S. Choi G. Plant Cell. 2011; 23: 1404-1415Crossref PubMed Scopus (105) Google Scholar). Upon activation by red light, phytochrome B is translocated to the nucleus, where it interacts with and causes the degradation of PIL5, preventing the accumulation of SOM transcript. This PHYB-PIL5-SOM pathway has been well defined by previous studies (see Oh et al., 2009Oh E. Kang H. Yamaguchi S. Park J. Lee D. Kamiya Y. Choi G. Plant Cell. 2009; 21: 403-419Crossref PubMed Scopus (289) Google Scholar and references therein). The direct mechanistic connection of PHYB-PIL5-SOM signaling to the regulation of GA levels, however, has remained elusive (Kim et al., 2008Kim D.H. Yamaguchi S. Lim S. Oh E. Park J. Hanada A. Kamiya Y. Choi G. Plant Cell. 2008; 20: 1260-1277Crossref PubMed Scopus (238) Google Scholar). Cho et al., 2012Cho J.-N. Ryu J.-Y. Jeong Y.-M. Park J. Song J.-J. Amasino R.M. Noh B. Noh Y.-S. Dev. Cell. 2012; 22 (this issue): 736-748Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar now show that the phytochrome B-mediated induction of GA3ox1 and GA3ox2 transcript accumulation is reduced in the jmj20-1 jmj22-1 double mutant, suggesting that JMJ20 and JMJ22 may act as the mechanistic "bridge" between the PHYB-PIL5-SOM pathway and GA-induced seed germination. The authors connect those two by demonstrating that SOM acts as a transcriptional repressor of the HR demethylases JMJ20 and JMJ22. When SOM is downregulated, JMJ20 and JMJ22 are upregulated. Cho et al. further show that JMJ20 and JMJ22 demethylate repressive dimethylated histone H4 arginine 3s (H4R3me2s) in the chromatin region of GA3ox1 and GA3ox2, leading to increased transcript accumulation. GA3ox1 and GA3ox2 are metabolic enzymes associated with generating bioactive GAs, which then leads to seed germination. This wonderful cascade of events, which includes light-mediated changes in protein confirmation and nuclear localization, protein interactions promoting repressor degradation, and the stimulation of epigenetic histone demethylation, leads to phytochrome B-mediated increases in GA levels and seed germination. Of course, the story is not complete. We still don't understand how H4R3me2s repress gene expression. Other epigenetic components associated with this phenomenon are out there waiting to be discovered, as are other targets of regulation for this pathway. In addition, there must be other JMJ20- and JMJ22-mediated sites of demethylation that have yet to be identified. Nonetheless, we have come a long way in the past 60 years, from observing red-light-stimulated seed germination in Grand Rapids lettuce to linking photomorphogenic- and hormone-mediated signaling pathways. Control of Seed Germination by Light-Induced Histone Arginine Demethylation ActivityCho et al.Developmental CellApril 5, 2012In BriefLight stimulates seed germination in part by suppressing expression of the transcriptional repressor SOMNUS. Cho et al. find two key SOMNUS target genes derepressed by light, JMJ20/JMJ22. The JMJ20/JMJ22 histone arginine demethylases act directly on GA3ox1/GA3ox2 to stimulate histone H4R3 demethylation, gibberellic acid production, and seed germination. Full-Text PDF Open Archive
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